Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-09T01:08:42.440Z Has data issue: false hasContentIssue false
  • English
  • Français

Gregarine infection accelerates larval development of the cat flea Ctenocephalides felis (Bouché)

Published online by Cambridge University Press:  11 January 2017

M. E. ALARCÓN ,
A. JARA-F. ,
R. C. BRIONES ,
A. K. DUBEY  and
C. H. SLAMOVITS
M. E. ALARCÓN
Affiliation:
Liceo Alemán del Verbo Divino Lynch 350 Los Ángeles, Bío-Bío, Chile
A. JARA-F.
Affiliation:
Doctorado en Sistemática y Biodiversidad, Departamento Zoología, Facultad de Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile
R. C. BRIONES
Affiliation:
División Manejo Ecosistémico, Programa Conservación de Fauna, Bioforest S.A. Concepción, Chile
A. K. DUBEY*
Affiliation:
Forest Entomology Division, Forest Research Institute, Dehradun, India
C. H. SLAMOVITS
Affiliation:
Canadian Institute for Advanced Research and Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, Nova Scotia, Canada
*
*Corresponding author: Forest Entomology Division, Forest Research Institute, New Forest, Dehradun, Uttarakhand, India. E-mail: anil2kd@yahoo.com
Get access Rights & Permissions [Opens in a new window]

Summary

A high degree of specialization between host and parasite is a well-known outcome of a long history of coevolution, and it is strikingly illustrated in a coordination of their life cycles. In some cases, the arms race ensued at the establishment of a symbiotic relationship results in the adoption of manipulative strategies by the parasite. We have already learned that Steinina ctenocephali, a gregarine living in the alimentary canal of cat flea, Ctenocephalides felis follows its phenology and metamorphosis. Despite these findings the outcome of their symbiotic partnership (mutualist, parasitic or commensal) remains unclear. To address this important question, we measured life history parameters of the flea in the presence of varying infection intensities of gregarine oocysts in laboratory conditions. We found that neither the emergence nor survival rate of fleas was affected by harbouring the gregarines. More surprisingly, our results show that flea larvae infected with gregarines developed faster and emerged earlier than the control group. This gregarine therefore joins the selected group of protists that can modify physiological host traits and provides not only new model taxa to be explored in an evolutionary scenario, but also potential development of control strategies of cat flea.

Keywords

Ctenocephalides felisSteinina ctenocephalioocyst concentrationsurvival curveflea development
Type
Research Article
Information
Parasitology , Volume 144 , Issue 4 , April 2017 , pp. 419 - 425
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alarcón, M. E., Huang, C. G., Tsai, Y. S., Chen, W. J., Dubey, A. K. and Wu, W. J. (2011). Life cycle and morphology of Steinina ctenocephali (Ross 1909) comb. nov. (Eugregarinorida: Actinocephalidae), a gregarine of Ctenocephalides felis (Siphonaptera: Pulicidae) in Taiwan. Zoological Studies 50, 763–772.Google Scholar
Alarcón, M. E., Huang, C. G., Dubey, A. K. and Benitez, H. A. (2013). A gregarine from the gut of cat flea, Ctenocephalides felis (Bouche) (Siphonaptera: Pulicidae) in Taiwan: dynamic of infection patterns. Veterinary Parasitology 192, 51–56.Google Scholar
Barnard, C. J. and Behnke, J. M. (1990). Parasitism and Host Behaviour. Taylor and Francis Publisher, London, UK.Google Scholar
Beard, C. B., Butler, J. F. and Hall, D. W. (1990). Prevalence and biology of endosymbionts of fleas (Siphonaptera: Pulicidae) from dogs and cats in Alachua County, Florida. Journal of Medical Entomology 27, 1050–1061.Google Scholar
Bossard, R. L., Dryden, M. W. and Broce, A. B. (2002). Insecticide susceptibilities of cat fleas (Siphonaptera : Pulicidae) from several regions of the United States. Journal of Medical Entomology 39, 742–746.CrossRefGoogle ScholarPubMed
Cleveland, L. R. (1959). Sex induced with ecdysone. Proceedings of the National Academy of Sciences of the United States of America 45, 747–753.Google Scholar
Corbel, J. C. (1964). Infestations expérimentales de Locusta migratoria L. (insecte orthoptère) par Gregarina garnhami Canning (Sporozoaire gregarinomorphe): relation entre le cycle de l'hôte et celui du parasite. Comptes Rendus de l'Académie des Sciences . Biologies 259, 207–210.Google Scholar
De Avelar, D. M. and Linardi, P. M. (2008). Seasonality and prevalence rates of Steinina sp. (Eugregarinorida: Actinocephalidae) in Ctenocephalides felis felis (Siphonaptera: Pulicidae) from dogs captured in Belo Horizonte, Minas Gerais, Brazil. Journal of Medical Entomology 45, 1139–1142.Google Scholar
Dubremetz, J. F., Garcia-Reguet, N., Conseil, V. and Fourmaux, M. N. (1998). Apical organelles and host-cell invasion by Apicomplexa. International Journal for Parasitology 28, 1007–1013.Google Scholar
Egerter, D. E., Anderson, J. R. and Washburn, J. O. (1986). Dispersal of the parasitic ciliate Lambornella clarki: implications for ciliates in the biological control of mosquitoes. Proceedings of the National Academy of Sciences of the United States of America 83, 7335–7339.Google Scholar
Griffiths, J. K., Moore, R., Dooley, S., Keusch, G. T. and Tzipori, S. (1994). Cryptosporidium parvum infection of Caco-2 cell monolayers induces an apical monolayer defect, selectively increases transmonolayer permeability, and causes epithelial cell death. Infection and Immunity 62, 4506–4514.Google Scholar
Henderson, G., Manweiler, S. A., Lawrence, W. J., Tempelman, R. J. and Foil, L. D. (1995). The effects of Steinernema carpocapsae (Weiser) application to different life stages on adult emergence of the cat flea Ctenocephalides felis (Bouche). Veterinary Dermatology 6, 159–163.CrossRefGoogle ScholarPubMed
Heussler, V. T., Kuenzi, P. and Rottenberg, S. (2001). Inhibition of apoptosis by intracellular protozoan parasites. International Journal for Parasitology 31, 1166–1176.Google Scholar
Hsu, Y. C. (2000). Effects of diet factors on larval development and survival of cat fleas, Ctenocephalides felis (Bouché) (Siphonaptera: Pulicidae) . Master thesis. National Taiwan University, Taipei (in Chinese, English [abstract]), 101 pp.Google Scholar
Hsu, M. H. and Wu, W. J. (2000). Effects of multiple mating on female reproductive output in the cat flea (Siphonaptera: Pulicidae). Journal of Medical Entomology 37, 828–834.Google Scholar
Hsu, M. H., Hsu, Y. C. and Wu, W. J. (2002). Consumption of flea faeces and eggs by larvae of the cat flea, Ctenocephalides felis . Medical and Veterinary Entomology 16, 445–447.Google Scholar
Koella, J. C., Rieu, L. and Paul, R. (2002). Stage-specific manipulation of a mosquito's host-seeking behaviour by the malaria parasite Plasmodium gallinaceum. Behav. Behavioural Ecology 13, 816–820.Google Scholar
Lagrue, C. and Poulin, R. (2010). Manipulative parasites in the world of veterinary science: implications for epidemiology and pathology. Veterinary Journal 184, 9–13.Google Scholar
Leander, B. S. (2008). Marine gregarines: evolutionary prelude to the apicomplexan radiation? Trends in Parasitology 24, 60–67.CrossRefGoogle Scholar
Malavasi, A. (1976). Relationships between the gregarine Schneideria schneiderae and its host Trichosia pubescens (Diptera, Sciaridae). Journal of Invertebrate Pathology 28, 363–371.Google Scholar
McCole, D. F., Eckmann, L., Laurent, F. and Kagnoff, M. F. (2000). Intestinal epithelial cell apoptosis following Cryptosporidium parvum infection. Infection and Immunity 68, 1710–1713.Google Scholar
McCoy, C., Broce, A. B. and Dryden, M. W. (2008). Flea blood feeding patterns in cats treated with oral nitenpyram and the topical insecticides imidacloprid, fipronil and selamectin. Veterinary Parasitology 156, 293–301. Epub 2008 May 23.CrossRefGoogle ScholarPubMed
Nowlin, N. (1922). Correlation of the life cycle of a parasite with the metamorphosis of its host. Journal of Parasitology 8, 153–160.Google Scholar
Porchet-Henneré, E. (1969). Corrélations entre le cycle d'une Coccidie: Coelotropha durchoni Vivier, et celui de son hôte Nereis diversicolor O. F. Müller (Annélide Polychète). Zeitschrift für Parasitenkunde 31, 299–314.Google Scholar
Poulin, R. (1994). The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology 109, 109–118.CrossRefGoogle ScholarPubMed
Prensier, G., Dubremetz, J. F. and Schrevel, J. (2008). The unique adaptation of the life cycle of the coelomic gregarine Diplauxis hatti to its host Perinereis cultrifera (Annelida, Polychaeta): an experimental and ultrastructural study. Journal of Eukaryotic Microbiology 55, 541–553.Google Scholar
Ross, E. (1909). A gregarine parasitic in the dog-flea Ctenocephalus serraticeps . Annals of Tropical Medicine and Parasitology 2, 359–363.Google Scholar
Rothschild, M. and Ford, B. (1964). Maturation and egg-laying of the rabbit flea (Spilopsyllus cuniculi Dale) induced by the external application of hydrocortisone. Nature 203, 210–211.Google Scholar
Rueckert, S., Chantangsi, C. and Leander, B. S. (2010). Molecular systematics of marine gregarines (Apicomplexa) from North-eastern Pacific polychaetes and nemerteans, with descriptions of three novel species: Lecudina phyllochaetopteri sp. nov., Difficilina tubulani sp. nov. and Difficilina paranemertis sp. nov. International Journal of Systematic and Evolutionary Microbiology 60, 2681–2690.Google Scholar
Rust, M. K., Hinkle, N. C., Waggoner, M., Mencke, N., Hansen, O. and Vaughn, M. B. (2001). The influence of imidacloprid on adult cat flea feeding. Compendium on Continuing Education for the Practicing Veterinarian 23, 18–21.Google Scholar
Singh, S. and Chitnis, C. E. (2012). Signalling mechanisms involved in apical organelle discharge during host cell invasion by apicomplexan parasites. Microbes and Infection/Institut Pasteur 14, 820–824.CrossRefGoogle ScholarPubMed
Sneller, V. P. (1979). Inhibition of Dirofilaria immitis in gregarine-infected Aedes aegypti preliminary observations. Journal of Invertebrate Pathology 34, 62–70.Google Scholar
Templeton, T. J., Enomoto, S., Chen, W. J., Huang, C. G., Lancto, C. A., Abrahamsen, M. S. and Zhu, G. (2010). A genome-sequence survey for Ascogregarina taiwanensis supports evolutionary affiliation but metabolic diversity between a Gregarine and Cryptosporidium . Molecular Biology and Evolution 27, 235–248.Google Scholar
Terry, R. S., Smith, J. E., Sharpe, R. G., Rigaud, T., Littlewood, D. T., Ironside, J. E., Rollinson, D., Bouchon, D., MacNeil, C., Dick, J. T. A. and Dunn, A. M. (2004). Widespread vertical transmission and associated host sex-ratio distortion within the eukaryotic phylum Microspora. Proceedings of the Royal Society of London Series B, Biological Sciences 271, 1783–1789.Google Scholar
Thomas, R. E., Wallenfels, L. and Popiel, I. (1996). On-host viability and fecundity of Ctenocephalides felis (Siphonaptera: Pulicidae), using a novel chambered flea technique. Journal of Medical Entomology 33, 250–256.Google Scholar
Valigurová, A. (2012). Sophisticated adaptations of Gregarina cuneata (Apicomplexa) feeding stages for epicellular parasitism. PLoS ONE 7, e42606. Epub 2012 August 10.Google Scholar
Webster, J. P. and Brunton, C. F. A. (1994). Macdonald DW. Effect of Toxoplasma gondii upon neophobic behaviour in wild brown-rats, Rattusm norvegicus . Parasitology 109, 37–43.Google Scholar
Zuk, M. (2008). The effects of gregarine parasites on longevity, weight loss, fecundity and developmental time in the field crickets Gryllus veletis and G. pennsylvanicus . Ecological Entomology 12, 349–354.Google Scholar
Supplementary material: File

Alarcón supplementary material

Alarcón supplementary material 1

Download Alarcón supplementary material(File)
File 11.7 KB

Alarcón supplementary material

Alarcón supplementary material 2

Download Alarcón supplementary material(Video)
Video 17.7 MB
Supplementary material: Image

Alarcón supplementary material

Alarcón supplementary material 3

Download Alarcón supplementary material(Image)
Image 7.1 MB